Switch in FGF signalling initiates glial differentiation in the Drosophila eye

Franzdóttir, Sigríður Rut; Engelen, Daniel; Yuva-Aydemir, Yeliz; Schmidt, Imke; Aho, Annukka; Klämbt, Christian

doi:10.1038/nature08167

Cited by 121 publications

(194 citation statements)

References 30 publications

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“…In wild type, glial cells are born in the optic stalk and migrate onto the eye imaginal disc during the third-instar larval stage (Choi and Benzer, 1994;Rangarajan et al, 1999;Silies et al, 2007). Glial cells move until they contact the nascent photoreceptor axons two to four cell rows behind the morphogenetic furrow (Franzdó ttir et al, 2009) (Fig. 2A) (Fig.…”

Section: Spinster Expression In the Eye Disc Gliamentioning

confidence: 99%

“…Since the activity of several signaling pathways known to be required for glial migration is affected by the sorting of membrane receptors and ligands into different endosomal compartments (Fischer et al, 2006), we assayed their potential interaction with Spinster. Recently, we could show that the eye disc glia expresses the FGF receptor Heartless (Htl) whose activation is pivotal in controlling glial development (Franzdó ttir et al, 2009). However, no change in Htl expression level or localization is detected in spinster mutants nor did we detect changed MAPK (mitogen-activated protein kinase)/[ERK (extracellular signal-regulated kinase)] phosphorylation in spinster MARCM clones (data not shown).…”

Section: Spinster Affects Endocytosismentioning

confidence: 99%

“…Photoreceptor neurons are sequentially generated in the wake of the morphogenetic furrow, which sweeps anteriorly over the eye imaginal disc. Thus, glial migration must be closely coupled to eye disc development (Choi and Benzer, 1994;Rangarajan et al, 1999;Silies et al, 2007Franzdó ttir et al, 2009). …”

Section: Introductionmentioning

confidence: 99%

“…On these cells, the perineurial glial cells migrate toward the morphogenetic furrow. At the anterior end of the carpet cell, the perineurial glial cells first contact nascent photoreceptor axons, which triggers the differentiation of the wrapping glia (Silies et al, 2007Franzdó ttir et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

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Spinster Controls Dpp Signaling during Glial Migration in theDrosophilaEye

Yuva-Aydemir¹,

Bauke²,

Klämbt³

2011

J. Neurosci.

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The development of multicellular organisms requires the well balanced and coordinated migration of many cell types. This is of particular importance within the developing nervous system, where glial cells often move long distances to reach their targets. The majority of glial cells in the peripheral nervous system of the Drosophila embryo is derived from the CNS and migrates along motor axons toward their targets. In the developing Drosophila eye, CNS-derived glial cells move outward toward the nascent photoreceptor cells, but the molecular mechanisms coupling the migration of glial cells with the growth of the eye imaginal disc are mostly unknown. Here, we used an enhancer trap approach to identify the gene spinster, which encodes a multipass transmembrane protein involved in endosome-lysosome trafficking, as being expressed in many glial cells. spinster mutants are characterized by glial overmigration. Genetic experiments demonstrate that Spinster modulates the activity of several signaling cascades. Within the migrating perineurial glial cells, Spinster is required to downregulate Dpp (Decapentaplegic) signaling activity, which ceases migratory abilities. In addition, Spinster affects the growth of the carpet cell, which indirectly modulates glial migration.

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Section: Spinster Expression In the Eye Disc Gliamentioning

confidence: 99%

Section: Spinster Affects Endocytosismentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Spinster Controls Dpp Signaling during Glial Migration in theDrosophilaEye

Yuva-Aydemir¹,

Bauke²,

Klämbt³

2011

J. Neurosci.

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“…First, R8 axons must navigate to the posterior of the eye disk and enter the optic stalk. This process is facilitated, in part, by retinal basal glial cells at the posterior edge of the eye disk (20,21). If glial cells are displaced anteriorly, R-cell axon fascicles project away from the optic stalk rather than toward it (21).…”

Section: Posterior R8 Axon Guidance Plays a Crucial Role In Axon Fascmentioning

confidence: 99%

Robo-3–mediated repulsive interactions guide R8 axons during Drosophila visual system development

Pappu

Morey

Nern

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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The formation of neuronal connections requires the precise guidance of developing axons toward their targets. In the Drosophila visual system, photoreceptor neurons (R cells) project from the eye into the brain. These cells are grouped into some 750 clusters comprised of eight photoreceptors or R cells each. R cells fall into three classes: R1 to R6, R7, and R8. Posterior R8 cells are the first to project axons into the brain. How these axons select a specific pathway is not known. Here, we used a microarray-based approach to identify genes expressed in R8 neurons as they extend into the brain. We found that Roundabout-3 (Robo3), an axon-guidance receptor, is expressed specifically and transiently in R8 growth cones. In wild-type animals, posterior-most R8 axons extend along a border of glial cells demarcated by the expression of Slit, the secreted ligand of Robo3. In contrast, robo3 mutant R8 axons extend across this border and fasciculate inappropriately with other axon tracts. We demonstrate that either Robo1 or Robo2 rescues the robo3 mutant phenotype when each is knocked into the endogenous robo3 locus separately, indicating that R8 does not require a function unique to the Robo3 paralog. However, persistent expression of Robo3 in R8 disrupts the layer-specific targeting of R8 growth cones. Thus, the transient cellspecific expression of Robo3 plays a crucial role in establishing neural circuits in the Drosophila visual system by selectively regulating pathway choice for posterior-most R8 growth cones.A striking feature of the insect visual system is the organization of neurons into parallel, interconnected layers and orthogonal columns that contain the axonal and dendritic processes from many neurons (1). Columnar organization preserves the topology of visual space. This organization is achieved, in part, during development by the assembly of axons into discrete fascicles. The fly eye comprises some 750 ommatidia or simple eyes, each containing a cluster of eight photoreceptor neurons (R1-R8). R-cell axons form a topographic map of the visual world in the lamina and medulla. The R1 to R6 axons terminate in the lamina, and R7 and R8 extend through the lamina and terminate in the medulla. Axons from each ommatidium form a discrete fascicle and form connections within columnar units, referred to as cartridges and columns in the lamina and medulla, respectively. The orderly assembly of cartridges and columns relies upon the precise spatiotemporal pattern of R-cell innervation.Two features of early eye development facilitate the orderly assembly of the visual system. First, individual rows of ommatidia are recruited sequentially, following a wave of differentiation beginning at the posterior margin of the eye primordium or eye disk and progressing anteriorly across it. As new ommatidia form, the R cells within them extend axons into the brain. Thus, the wave of ommatidial formation is converted into sequential innervation of the brain (2). Second, R cells in the same developing ommatidium extend axons within a s...

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Glioblastoma Models in Drosophila Melanogaster

Jeibmann

Sn²,

Paulus

et al. 2010

Encyclopedia of Life Sciences

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Gliomas comprise the most common and most malignant intrinsic human brain tumours, with a very poor prognosis. Despite some recent therapeutic progress, there is still a large demand for novel drug targets to cope with the high recurrence rate. In the present article, we introduce the Drosophila model as a new tool in deciphering the mechanisms underlying the generation and progression of glial tumours. Despite the fact that Drosophila has only few glial cells and no vascular system with patrolling lymphocytes, the basic principles underlying glioblastoma biology appear very well conserved. The role of epidermal growth factor (EGF) receptor pathways, PVR (PDGF‐ and VEGF‐receptor related) and phophatidylinositol 3‐kinase (PI3K) signalling in Drosophila glioma models is discussed. Key Concepts: Gliomas are the most common and most malignant intrinsic human brain tumours, with a very poor prognosis. In majority of the glioblastoma, the molecular cause of malignancy is due to an amplification of receptor tyrosine kinase genes. The role of EGF‐receptor pathways, PVR and PI3K signalling in Drosophila glioma models is introduced in the text. Glial cell proliferation and glial cell migration is controlled by evolutionary conserved mechanisms. The insect Drosophila melanogaster has a very simple structured nervous and glial cells perform similar tasks as their vertebrate counterparts. The model organism Drosophila provides a rich source to decipher the mechanisms underlying the biology of human glioma and can be used to define novel drug targets.

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Switch in FGF signalling initiates glial differentiation in the Drosophila eye

Cited by 121 publications

References 30 publications

Spinster Controls Dpp Signaling during Glial Migration in theDrosophilaEye

Spinster Controls Dpp Signaling during Glial Migration in theDrosophilaEye

Robo-3–mediated repulsive interactions guide R8 axons during Drosophila visual system development

Glioblastoma Models in Drosophila Melanogaster

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